Nitrite oxidation in the upper water column and oxygen minimum zone of the eastern tropical North Pacific Ocean

Beman, J. Michael; Shih, Joy L.; Popp, Brian N.

doi:10.1038/ismej.2013.96

Cited by 108 publications

(168 citation statements)

References 62 publications

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“…Proteins catalyzing the second step of nitrification, nitrite oxidase (NXR), from N. graclilis and N. defluvii followed the same pattern of expression as Amo. Moreover, the detection of both Amo and NXR from nitrifying taxa, albeit at lower NSAF values in the SNTZ and SZ, supports recent observations of NO 2 − oxidation in the Namibian OMZ with implications for NO 3 − supply for denitrification (28,33). Nitrite oxidase from Planctomycetes ( Fig.…”

Section: Resultssupporting

confidence: 68%

Metaproteomics reveals differential modes of metabolic coupling among ubiquitous oxygen minimum zone microbes

Hawley¹,

Brewer

Norbeck

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

162

193

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Marine oxygen minimum zones (OMZs) are intrinsic water column features arising from respiratory oxygen demand during organic matter degradation in stratified waters. Currently OMZs are expanding due to global climate change with resulting feedback on marine ecosystem function. Here we use metaproteomics to chart spatial and temporal patterns of gene expression along defined redox gradients in a seasonally stratified fjord to better understand microbial community responses to OMZ expansion. The expression of metabolic pathway components for nitrification, anaerobic ammonium oxidation (anammox), denitrification, and inorganic carbon fixation were differentially expressed across the redoxcline and covaried with distribution patterns of ubiquitous OMZ microbes including Thaumarchaeota, Nitrospina, Nitrospira, Planctomycetes, and SUP05/ARCTIC96BD-19 Gammaproteobacteria. Nitrification and inorganic carbon fixation pathways affiliated with Thaumarchaeota dominated dysoxic waters, and denitrification, sulfur oxidation, and inorganic carbon fixation pathways affiliated with the SUP05 group of nitrate-reducing sulfur oxidizers dominated suboxic and anoxic waters. Nitrifier nitrite oxidation and anammox pathways affiliated with Nirospina, Nitrospira, and Planctomycetes, respectively, also exhibited redox partitioning between dysoxic and suboxic waters. The numerical abundance of SUP05 proteins mediating inorganic carbon fixation under anoxic conditions suggests that SUP05 will become increasingly important in global ocean carbon and nutrient cycling as OMZs expand.M arine oxygen (O 2 ) minimum zones (OMZs) are widespread and naturally occurring water column features that arise when respiratory O 2 demand during decomposition of organic matter exceeds O 2 availability in stratified waters. Operationally defined by dissolved O 2 concentrations <20 μM, OMZs promote the use of alternative terminal electron acceptors (TEAs) in microbial energy metabolism that results in climate active gas production including carbon dioxide (CO 2 ), nitrous oxide (N 2 O), and methane (CH 4 ) (1). Currently, OMZs constitute ∼7% of the ocean volume (1, 2). However, global warming promotes conditions for OMZ expansion and intensification, e.g., reduced O 2 solubility and increased stratification, with resulting feedback on the climate system (3, 4).Within OMZs, the use of nitrate (NO 3 − ) and nitrite (NO 2 − ) as TEAs in dissimilatory nitrate reduction (denitrification) and anaerobic ammonium oxidation (anammox) results in fixed nitrogen loss in the form of N 2 O and dinitrogen gas (N 2 ), respectively (5, 6). Because OMZs account for up to 50% of oceanic N 2 production, they have the potential to limit primary production in overlying surface waters (7,8). A recent model suggests that nitrogen fixation in proximity to OMZ waters can balance nitrogen loss processes (9), and several studies along redoxclines in the Eastern Tropical South Pacific and Baltic Sea have measured nitrogen fixation rates that support a close spatial coupling between nitro...

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Section: Resultssupporting

confidence: 68%

Metaproteomics reveals differential modes of metabolic coupling among ubiquitous oxygen minimum zone microbes

Hawley¹,

Brewer

Norbeck

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

162

193

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“…2). A high-affinity component for nitrite oxidation, and hence nitrite oxidation having a higher affinity for low nanomolar oxygen than that observed for ammonium oxidation, aligns with the typical depth distribution of AOA and nitrite-oxidizing bacteria (NOB) observed in OMZs, where NOB are typically distributed deeper and at higher abundances into the OMZ core relative to AOA (17,49).…”

Section: Resultsmentioning

confidence: 62%

Ammonium and nitrite oxidation at nanomolar oxygen concentrations in oxygen minimum zone waters

Bristow

Dalsgaard

Tiano

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

202

209

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A major percentage of fixed nitrogen (N) loss in the oceans occurs within nitrite-rich oxygen minimum zones (OMZs) via denitrification and anammox. It remains unclear to what extent ammonium and nitrite oxidation co-occur, either supplying or competing for substrates involved in nitrogen loss in the OMZ core. Assessment of the oxygen (O 2 ) sensitivity of these processes down to the O 2 concentrations present in the OMZ core (<10 nmol·L −1 ) is therefore essential for understanding and modeling nitrogen loss in OMZs. We determined rates of ammonium and nitrite oxidation in the seasonal OMZ off Concepcion, Chile at manipulated O 2 levels between 5 nmol·L −1 and 20 μmol·L −1 . Rates of both processes were detectable in the low nanomolar range (5-33 nmol·L −1 O 2 ), but demonstrated a strong dependence on O 2 concentrations with apparent half-saturation constants (K m s) of 333 ± 130 nmol·L −1 O 2 for ammonium oxidation and 778 ± 168 nmol·L −1 O 2 for nitrite oxidation assuming one-component Michaelis-Menten kinetics. Nitrite oxidation rates, however, were better described with a two-component Michaelis-Menten model, indicating a high-affinity component with a K m of just a few nanomolar. As the communities of ammonium and nitrite oxidizers were similar to other OMZs, these kinetics should apply across OMZ systems. The high O 2 affinities imply that ammonium and nitrite oxidation can occur within the OMZ core whenever O 2 is supplied, for example, by episodic intrusions. These processes therefore compete with anammox and denitrification for ammonium and nitrite, thereby exerting an important control over nitrogen loss.is a key factor regulating biogeochemical cycling in the marine environment (1). Although the vast majority of the ocean remains well oxygenated, subsurface regions of extreme oxygen depletion can persist along eastern boundaries of the world's ocean basins. These regions are known as oxygen minimum zones (OMZs) and are located within the eastern tropical North and South Pacific, the Arabian Sea, and off the coast of Namibia, where oxygen depletion results from poor ventilation and a high export of organic matter from productive surface waters, generating high rates of subsurface oxygen consumption (2, 3).Oceanic waters characterized by oxygen-deficient conditions (<4.5 μmol·L −1 O 2 ) account for <0.1% of total ocean volume but for >30% of fixed nitrogen (N) loss (3-6) due to the onset of anaerobic processes, including denitrification and anammox (7-10). Both field and modeling observations point to the expansion of low oxygen regions as a result of global warming (11). Thus, to evaluate the biogeochemical impact of these regions, it is imperative to understand fully how oxygen controls the cycling of substrates involved in nitrogen loss pathways.Recent studies have quantified the oxygen sensitivity of anaerobic OMZ nitrogen transformations, finding that denitrification has relatively low oxygen tolerance with a half-inhibition concentration (IC 50 ) of 0.3 μmol·L −1 , compared with higher values for...

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“…ARCTIC96BD-19 reached comparable abundances in the ETNP OMZ (up to 16.5%), but SUP05 and Sulfurimonas were less abundant (o0.4%). Nitrospina 16S rRNA genes formed up to 9% of libraries and correlated with quantitative PCR data (r 2 ¼ 0.79, Po0.05), while nitrite oxidation was detected at the same depths where Nitrospina were numerous 27 . These data indicate that the relative proportions of bacteria within pyrosequencing libraries accurately reflect their proportions within the water column, and, together with amplification of 16S rRNA, are indicative of activity in the ETNP OMZ.…”

Section: Trends In Domentioning

confidence: 92%

“…Third, N-cycling processes have well-documented sensitivity to DO and light that may be affected by OMZ shoaling. The high abundance of Nitrospina and high rates of nitrite oxidation within the OMZ may be affected by light 27 , potentially altering the form and availability of N for anaerobic processes in the OMZ (for example, decreasing the re-oxidation of nitrite back to nitrate). Fourth, S oxidation appears to be an important ecosystem service provided by microbes in OMZs 5 , and our data suggest that the composition of S-oxidizers changes with simulated deoxygenation.…”

Section: Discussionmentioning

confidence: 99%

Deoxygenation alters bacterial diversity and community composition in the ocean’s largest oxygen minimum zone

Beman

Carolan

2013

Nat Commun

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Oceanic oxygen minimum zones (OMZs) have a central role in biogeochemical cycles and are expanding as a consequence of climate change, yet how deoxygenation will affect the microbial communities that control these cycles is unclear. Here we sample across dissolved oxygen gradients in the oceans' largest OMZ and show that bacterial richness displays a unimodal pattern with decreasing dissolved oxygen, reaching maximum values on the edge of the OMZ and decreasing within it. Rare groups on the OMZ margin are abundant at lower dissolved oxygen concentrations, including sulphur-cycling Chromatiales, for which 16S rRNA was amplified from extracted RNA. Microbial species distribution models accurately replicate community patterns based on multivariate environmental data, demonstrate likely changes in distributions and diversity in the eastern tropical North Pacific Ocean, and highlight the sensitivity of key bacterial groups to deoxygenation. Through these mechanisms, OMZ expansion may alter microbial composition, competition, diversity and function, all of which have implications for biogeochemical cycling in OMZs.

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Nitrite oxidation in the upper water column and oxygen minimum zone of the eastern tropical North Pacific Ocean

Cited by 108 publications

References 62 publications

Metaproteomics reveals differential modes of metabolic coupling among ubiquitous oxygen minimum zone microbes

Metaproteomics reveals differential modes of metabolic coupling among ubiquitous oxygen minimum zone microbes

Ammonium and nitrite oxidation at nanomolar oxygen concentrations in oxygen minimum zone waters

Deoxygenation alters bacterial diversity and community composition in the ocean’s largest oxygen minimum zone

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